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Phosphorylation of d-allose by hexokinase involved in regulation of OsABF1 expression for growth inhibition in Oryza sativa L.

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Abstract

We previously reported that a rare sugar d-allose, which is the d-glucose epimer at C3, inhibits the gibberellin-dependent responses such as elongation of the second leaf sheath and induction of α-amylase in embryo-less half seeds in rice (Fukumoto et al. 2011). d-Allose suppresses expressions of gibberellin-responsive genes downstream of SLR1 protein in the gibberellin-signaling through hexokinase (HXK)-dependent pathway. In this study, we discovered that d-allose induced expression of ABA-related genes including OsNCED1-3 and OsABA8ox1-3 in rice. Interestingly, d-allose also up-regulated expression of OsABF1, encoding a conserved bZIP transcription factor in ABA signaling, in rice. The d-allose-induced expression of OsABF1 was diminished by a hexokinase inhibitor, d-mannoheptulose (MNH). Consistently, d-allose also inhibited Arabidopsis growth, but failed to trigger growth retardation in the glucose-insensitive2 (gin2) mutant, which is a loss-of-function mutant of the glucose sensor AtHXK1. d-Allose activated AtABI5 expression in transgenic gin2 over-expressing wild-type AtHXK1 but not in gin2 over-expressing the catalytic mutant AtHXK1S177A, indicating that the d-allose phosphorylation by HXK to d-allose 6-phosphate (A6P) is the first step for the up-regulation of AtABI5 gene expression as well as d-allose-induced growth inhibition. Moreover, overexpression of OsABF1 showed increased sensitivity to d-allose in rice. These findings indicated that the phosphorylation of d-allose at C6 by hexokinase is essential and OsABF1 is involved in the signal transduction for d-allose-induced growth inhibition.

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Abbreviations

ABA:

Abscisic acid

A6P:

d-Allose 6-phosphate

GA:

Gibberellin

gin2 :

Glucose-insensitive2

HXK:

Hexokinase

MNH:

d-Mannoheptulose

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Acknowledgments

We thank Rice Genome Resource Center at National Institute of Agrobiological Sciences (NIAS, Tsukuba, Japan) for providing full-length cDNA used in this study. This study was supported by the Programme for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry.

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Authors and Affiliations

  1. Faculty of Agriculture, Rare Sugar Research Center, and Gene Research Center, Kagawa University, Miki, Kagawa, 761-0795, Japan

    Takeshi Fukumoto, Akihito Kano, Kouhei Ohtani, Megumi Inoue, Akihide Yoshihara, Ken Izumori, Shigeyuki Tajima, Yasuomi Tada, Kazuya Ichimura, Kenji Gomi & Kazuya Akimitsu

  2. Mitsui Chemicals Agro Co. Ltd, Yasu, Shiga, 520-2342, Japan

    Yoshio Shigematsu, Keiji Tanaka & Takeo Ohkouchi

  3. Shikoku Research Institute Inc, Takamatsu, Kagawa, 761-0192, Japan

    Yutaka Ishida

  4. National Institute of Agrobiological Sciences, Tsukuba, Ibaragi, 305-8602, Japan

    Yoko Nishizawa

  5. Department of Biological Sciences, SungKyunKwan University, Suwon, 440-746, Korea

    Sang-Dong Yoo

  6. Department of Molecular Biology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA

    Jen Sheen

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  1. Takeshi Fukumoto
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Correspondence to Kazuya Akimitsu.

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425_2013_1853_MOESM1_ESM.tif

Supplemental Fig. S1 Effect of 6-deoxy-d-allose on growth rate of rice seedlings. One microliter of 6-deoxy-d-allose (6-DA) solutions (10, 100, 500 and 1000 mM) was applied as the same methods described in Fig 1. The second sheath and shoot lengths were measured at 6 days after treatment, and compared to that of the water-treated control. All plants were grown at 25°C in growth chambers after the sugar treatment. Each datum is the average of 20 seedlings with SD values, and no statistical differences (P<0.05) found among respective data as indicated by same letter (TIFF 156 kb)

425_2013_1853_MOESM2_ESM.tif

Supplemental Fig. S2 HPLC detection of d-allose and d-allose 6-phosphate in extracts from Arabidopsis leaves. Total protein was extracted from plants (100 mg FW) of wild type Arabidopsis (WT), gin2 mutant, transgenic gin2 plant over-expressing normal AtHXK (gin2/35S::AtHXK1), and transgenic gin2 plant over-expressing point mutated AtHXK1 at S177A (gin2/35S::S177A) as described in Fig. 5, which was grown for 10 days on MS medium supplemented with 1 % sucrose. d-Allose and A6P were detected after coupled with p-aminobenzoic ethyl ester (ABEE) by the method of Yasuno et al. (1997) with modifications (TIFF 356 kb)

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Fukumoto, T., Kano, A., Ohtani, K. et al. Phosphorylation of d-allose by hexokinase involved in regulation of OsABF1 expression for growth inhibition in Oryza sativa L.. Planta 237, 1379–1391 (2013). https://doi.org/10.1007/s00425-013-1853-9

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